AOBPreview published online on July 27, 2007
Annals of Botany, doi:10.1093/aob/mcm148
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Resistance of Red Clover (Trifolium pratense) to the Root Parasitic Plant Orobanche minor is Activated by Salicylate but not by Jasmonate
1 Weed Science Center, Utsunomiya University, 350 Mine-machi, Utsunomiya 321-8505, Japan
2 R.H. Smith Institute of Plant Sciences & Genetics in Agriculture, Faculty of Agriculture, Food & Environmental Sciences, The Hebrew University of Jerusalem, Rehovot 76100, Israel
3 United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo 183-8509, Japan
* For correspondence. E-mail yoneyama{at}cc.utsunomiya-u.ac.jp
Received: 12 February 2007 Returned for revision: 21 May 2007 Accepted: 1 June 2007
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ABSTRACT |
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Background and Aims: Obligate root holoparasites of the genus Orobanche attack dicotyledonous crops and cause severe losses in many parts of the world. Chemical induction of plant defence systems such as systemic acquired resistance was proposed to be an available strategy to control the root parasite, but the detailed mechanisms involved have not been clarified. The aim of this study was to elucidate the effects of salicylic acid (SA), jasmonic acid (JA) and their analogues on resistance of red clover to Orobanche parasitism.
Methods: Roots of red clover grown in plastic chambers were applied with SA, S-methyl benzo[1,2,3]thiadiazole-7-carbothioate (BTH), methyl jasmonate (MeJA) and n-propyl dihydrojasmonate (PDJ), and then were inoculated with O. minor seeds. Attachments of the parasite were observed after 5 weeks.
Key Results: SA and BTH, inducers of SA-mediated defences, significantly reduced the number of established parasites by more than 75 %. By contrast, MeJA and PDJ, inducers of JA-mediated defences, did not affect parasitism. The reduction in the number of established parasites by SA and BTH was due to the inhibited elongation of O. minor radicles and the activation of defence responses in the host root including lignification of the endodermis.
Conclusions: These results suggest that SA-induced resistance, but not JA-induced resistance, is effective in inhibiting Orobanche parasitism and that the resistance is expressed by the host root both externally and internally.
Key words: Endodermis, haustorium inducing signal, induced resistance, jasmonic acid, lignification, Orobanche minor, root parasitic plant, salicylic acid, Trifolium pratense (red clover)
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Root parasitic plants of the genus Orobanche lack chlorophyll and depend on their host plants for the acquisition of nutrients and water. Orobanche spp. infest agriculturally important dicotyledonous crops and cause severe yield losses of their production in many parts of the world, especially the Mediterranean region (Parker and Riches, 1993). Orobanche aegyptiaca, O. ramosa, O. crenata, O. cumana and O. minor are economically damaging species. Several control strategies have been proposed and employed, but none has proved efficacious because of the complex interaction between hosts and parasites.
Salicylic acid (SA) is a chemical defence-inducer promoting fungal, bacterial and viral disease resistance and induces production of acidic pathogenesis-related proteins and hypersensitive responses in many plant species (Reymond and Farmer, 1998; Sudha and Ravishankar, 2002). S-methyl benzo[1,2,3]thiadiazole-7-carbothioate (BTH) is a synthetic functional analogue of SA (Görlach et al., 1996; Bokshi et al., 2003) and its application to plants has been proposed to be an applicable strategy to control Orobanche parasitism. For example, soaking of sunflower seeds in BTH solution reduced the number of attachments of O. cumana (Sauerborn et al., 2002). BTH soil drenching reduced the attachments of O. ramosa in hemp and tobacco (Gonsior et al., 2004) and O. cumana in sunflower (Müller-Stöver et al., 2005). Foliar spray of BTH was also reported to reduce O. crenata attachments in pea (Pérez-de-Luque et al., 2004). Although several reports have suggested the effectiveness of BTH application on the reduction of Orobanche attachments, physiological resistant mechanisms to Orobanche infestation induced by BTH have not been clarified.
Jasmonic acid (JA) is another defence-inducer promoting resistance against insects (McCorn et al., 1997) and pathogens (Thomma et al., 1998). JA induces production of proteinase inhibitors (Farmer and Ryan, 1990) and basic pathogenesis-related proteins in plants. Although the regulatory mechanisms and gene expression induced by JA are different from those induced by SA (Reymond and Farmer, 1998; Thomma et al., 1998), the effect of JA on resistance to root parasitic plants has not previously been demonstrated. The aim of the present study was to elucidate the effects and the inhibitory mechanism(s) of SA and JA on resistance to Orobanche parasitism.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Source of seeds
Orobanche minor Sm. seeds were collected from mature plants that parasitized red clover, grown in the Watarase basin in Japan in 2004. Seeds of red clover (Trifolium pratense L. ‘Makimidori’), a typical host of O. minor (Parker and Riches, 1993), were purchased from Snow Brand Seed Co., Ltd in Japan.
Plant material and growth conditions
Plastic chambers (14 cm in height x 10 cm in width x 1·5 cm in depth) with a 1-cm-wide rectangular hole in the centre of the top were filled with rockwool (Nitto Boseki Co. Ltd, Tokyo, Japan). A glass-fibre filter paper (14 x 10 cm; GC-90, ADVANTEC, Tokyo, Japan) was placed between the rockwool and the lid of the plastic chamber, and a small seedbed made of rockwool was put between the plastic lid and the glass-fibre filter paper near the hole (Fig. 1). The rockwool and the glass-fibre filter paper in the plastic chamber were moistened with tap water. Seeds of red clover were soaked in running tap water for 3 d and then one seed each was placed in the seedbed on the top, at the centre of the plastic chamber. The plastic chambers were wrapped with aluminium foil leaving the top part exposed and were incubated in a growth chamber at 23 °C with a 16-h photoperiod (photosynthetic photon flux densities of 52 µmol s–1 m–2). The red clover seeds germinated within 3 d under these growth conditions. The seedlings were replenished with tap water for the first 5 d, with half-strength Tadano–Tanaka medium (Tadano and Tanaka, 1980) for the next 6 d and then with tap water until the end of the experiments.
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Treatment with chemical defence-inducers and inoculation of O. minor seeds
Orobanche minor seeds were surface-sterilized in 70 % ethanol for 2 min and then in 1 % sodium hypochlorite solution for 2 min. Sterilized seeds were incubated in a sealed Petri dish lined with a filter paper moistened with distilled water at 23 °C in the dark for 7 d (seed conditioning).
The plastic chambers prepared as described above were opened and the red clover seedlings with the seedbeds and the glass-fibre filter papers were taken out from the chambers one month after cultivation. The seedlings were handled carefully so as not to separate them from the seedbeds and the glass-fibre filter papers. The red clover roots, the seedbeds and the glass-fibre filter papers were submerged in solutions of 0·2 mM SA, BTH, methyl jasmonate (MeJA) or n-propyl dihydrojasmonate (PDJ), a functional analogue of JA (Fujisawa et al., 1998), with 0·1 % Tween 20 for 3 h and then thoroughly rinsed with water to remove the unabsorbed chemicals. Control plants were treated with only 0·1 % Tween 20 solution in the same way. The conditioned O. minor seeds were transferred onto the glass-fibre filter papers so that they were in contact with the red clover roots, 15 seeds per 1 cm of the root. The glass-fibre filter papers were uniformly moistened with 1 mg L–1 GR24, a synthetic germination stimulant, to induce seed germination synchronously. The red clover seedlings, the seedbeds and the glass-fibre filter papers were returned to the plastic chambers and the seedlings were incubated at 23 °C with a 16-h photoperiod for 5 weeks. Five replications were prepared for each treatment.
Estimation of O. minor penetration
The number of O. minor seedlings attaching to red clover roots and their development stages were recorded 5 weeks after inoculation. Developmental stages were classified as follows: S1, radicle attaching to host root surface; S2, haustorium penetrating into host root without swelling of host root; S3, host root swelling at penetrated site; S4, formation of tubercle; and S5, tubercle with root-like structures (Fig. 2).
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Histological study
The red clover root sites of penetration by O. minor seedlings and tubercles were fixed with 10 % formaldehyde. After dehydration through a graded series of ethanol (50, 75, 95, 100, 100 %; 24 h), samples were embedded in LR white resin soft (Sigma, St Louis, MO, USA). Sections (5–10 µm) were cut with a rotary microtome (RM 2125RT; Leica Microsystems, Tokyo, Japan) and stained with safranin-fast green double staining (Johansen, 1940). With this staining method, cellulose and some cytoplasm are stained blue or green, while lignified cell walls, phenolic substances and nuclei appear red. Lignified cell walls were also detected with phloroglucinol-HCl (Jensen, 1962).
Direct effects of chemical defence-inducers on germination of O. minor seeds and elongation of radicles
Germination tests were conducted according to Chae et al. (2004). After conditioning of O. minor seeds, they were transferred to the 0·2 mM solutions of SA, BTH, MJ and PDJ with 1 mg L–1 GR24. Seed germination, length of radicles and morphology of root tips were observed after incubation for 7 d. Viability of the radicles was detected by staining with 0·4 % trypan blue. Four Petri dishes per treatment were prepared.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Induced resistance to O. minor infection by chemical defence-inducers
The number of O. minor seedlings that successfully parasitized red clover roots was reduced by 86 and 77 % by SA and BTH treatments, respectively (Fig. 1 and Table 1). It was found that this reduction was caused by a combination of two separate resistance mechanisms, namely the inhibited elongation of O. minor radicles and the increased resistance of host roots.
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SA treatment significantly reduced the total number of O. minor seedlings attaching to the red clover root (Table 1). As observed microscopically, germination of O. minor seeds was not different among the treatments (more than 80 %). However, directed growth of the parasite radicles toward the SA-treated red clover roots was inhibited (Fig. 3). The inhibited radicles had papillate cells on their root tips and some of them exhibited a bifurcate root tip form (Fig. 3). These morphologies seemed to be similar to that of attachment organs induced after root tips of Orobanche reach a host root under normal conditions (Joel and Losner-Goshen, 1994). When direct effects of the chemical defence-inducers on GR24-elicited seed germination and seedling growth of O. minor were examined, neither the germination rate nor the radicle elongation determined 7 d after GR24 treatment were affected by these defence-inducers. The root tips were smooth and conical, and did not develop to attachment organs in all the treatments. None of the seedlings exhibited pronounced reduction of cell viabilities as determined by staining with trypan blue. These results indicate that the reduction of the parasite attachments was not due to the direct effect of the chemicals on seed germination and radicle growth. Normally Orobanche radicles stop elongation soon after the root tips reach a host, and then form attachment organs. However, signals inducing attachment organ formation have not been identified, unlike similar parasitic plants Striga and Triphysaria (Yoder, 2001). Recently, it was noted that attachment organ differentiation in Orobanche was triggered endogenously in the absence of a host (González-Verdejo et al., 2005). Therefore, we presume that SA-treated red clover root interrupted radicle elongation via chemical interactions although relationship between the exudates from SA-treated roots and the differentiation of attachment organs remains uncertain.
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A second barrier to parasitism occurred after cortical invasion by the parasite but before gross morphological changes were observed in the host. Anatomical observations showed that the penetration of parasitic intrusive cells in stage S2 was stopped at the lignified endodermis of the host root and did not connect with host vessels (Fig. 4A, C). By contrast, parasites in stage S3–S5 penetrated into the central cylinder of the red clover root and the haustorial cells occupied the central cylinder of the host roots (Figs 5 and 6). In the later stages of S4 and S5, the haustoria expanded in the host root (Fig. 6A) and axially orientated xylem vessels of the parasite origin appeared together with the host vessels (Fig. 6B, C). Vertical parasite vessels linked with the axial parasite vessels were observed in the middle of the tubercle (Fig. 6B). These anatomical data suggest that O. minor seedlings in S2 failed in successive penetration into host vascular systems due to host resistance and those in S3–S5 successfully connected and infected the host root.
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The percentage of individual parasitism stages after parasitic cells invaded into red clover root (S2, S3, S4 and S5) was calculated to clarify further the effects of the chemical defence-inducers on internal resistance of the red clover root (Table 2). SA and BTH induced an increase in the percentage of the parasitic cells penetrating through the cortex but not into the central cylinder (S2) and decreased the percentage of the stages where the haustoria succeeded in penetrating into the central cylinder (S3 and S4). By contrast, MeJA and PDJ had little influence on these processes. These results suggest that SA and BTH activate defence responses in the red clover root and thus prevent the successful invasion of the parasite, whereas MeJA and PDJ have little effects on the resistance to the Orobanche penetration.
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Histological observations
A histological study of the infection site was performed to clarify the mechanism by which the host root prevented penetration of the parasite. The intrusive cells of O. minor in stage S2 penetrated through the epidermis and the cortex of the red clover root but further penetration was stopped at the endodermis (Fig. 4A). The boundary walls between the haustoria and the host cortex were brown in non-stained sections. In some cases, brown droplets accumulated in host fibres close to the parasitic intrusive cells. These droplets were stained by safranin (Fig. 4B) and phloroglucinol-HCl (Fig. 4C), suggesting that they contained lignin-like low-molecular-weight substances. The cell walls of the fibres that accumulated brown droplets were lignified (Fig. 4C). Thick vessel walls were formed near the parasitic intrusive cells and stained dense red by safranin and phloroglucinol-HCl (Fig. 4A), indicating that the walls were highly lignified. Some host vessels were occluded by a stained substance revealed by safranin-fast green (Fig. 4B). The phloroglucinol-HCl staining revealed lignification of the cell walls of the endodermis and the pericycle that contacted the parasitic intrusive cells, when the penetration stopped at the endodermis (Fig. 4C). In the more developed stages, S3–S5, the intrusive cells penetrated through the host endodermis into the central cylinder and haustoria occupied the inside (Figs 5 and 6). Host cells in the central cylinder were destroyed by the parasite except for host vessels and lignified fibre cells. Most of the host vessels either had lignified thick walls (Fig. 5B) or were occluded by a stained substance (Fig. 5D) such as those observed in S2. No anatomical differences elicited by the chemical treatments were observed as long as the observed sites were in the same stage of parasitism.
Before discussing the effects of SA and BTH on the resistance of the red clover roots to Orobanche, it is useful to summarize the three aspects of host root resistance during the early stages of the penetration. Cortical resistance is the first resistance that the penetrating haustoria encounter. It has often been represented as an apoplastic secretion of brown substances (Goldwasser et al., 2000; Rubiales et al., 2003). However, some reports indicated that this secretion originated from the parasite cells (Pérez-de-Luque et al., 2005). In more recent studies, suberization (Echevarría-Zomeño et al., 2006) and protein cross-linking (Echevarría-Zomeño et al., 2006; Pérez-de-Luque et al., 2006a) of the cortical cell walls have been suggested to be involved in the resistance. The haustoria then face endodermal resistance after passing through the cortex. A genotype of vetch with endodermal resistance (Goldwasser et al., 2000) exhibited higher accumulation of lignin in response to parasite infection than a susceptible genotype (Goldwasser et al., 1999). Anatomical studies revealed that lignification was induced in the endodermal and pericycle cells in contact with the parasitic intrusive cells (Maiti et al., 1984; Pérez-de-Luque et al., 2005, 2006b). The lignified cells are presumed to restrict the penetration of the parasite cells into the host central cylinder as a physical barrier. If the parasite penetrates through the endodermis before the lignification is induced or it overcomes the lignified barrier, vessel occlusion plays the role in resistance. After penetrating into the central cylinder, the parasite connects to host vascular systems and forms a tubercle. However, massive vessel occlusion by secretion of substances containing carbohydrates and polyphenols (Labrousse et al., 2001; Pérez-de-Luque et al., 2005, 2006b) and/or tylosis (Maiti et al., 1984) is assumed to diminish water and nutrient supply to the parasite and cause tubercle necrosis. These three resistant mechanisms depend on the genotype of host plants (Labrousse et al., 2001) and single or multiple mechanisms probably contribute to the resistance to the parasite penetration in a resistant genotype. By contrast, no or only weak resistant responses appeared in a susceptible genotype. In the present study, the non-treated red clover root exhibited the endodermal resistance in half of the penetration sites (see stage S2 in Table 2). SA and BTH treatment increased the percentage of penetration sites in stage S2, suggesting that these chemicals enhanced endodermal resistance, presumably through the activation of lignification (Table 2, Fig. 4C). On the other hand, no clear cortical resistance appeared in the roots treated with these chemicals. Although vessel resistance was shown as lignified thick walls and occlusion by substances, SA and BTH treatments did not affect the frequency of lignification of cell walls and vessel occlusion, nor the growth or necrosis of the tubercles. Therefore, it is likely that the main form of resistance enhanced by SA and BTH is endodermal resistance. The effects of SA on the synthesis of lignin are not fully understood (Reymond and Farmer, 1998), but some reports suggested that SA activated lignification in response to pathogen infection (Mauch-Mani and Slusarenko, 1996; He and Wolyn, 2005).
Possible strategy of Orobanche parasitism in host roots
The present results showed that SA-dependent defence responses effectively inhibited Orobanche parasitism on a host plant but JA-dependent defence responses had little effect. SA and JA induce different defence gene expression via independent signalling pathways (Reymond and Farmer, 1998). Recent reports described the defence gene expression of host plants infested by Orobanche spp. Based on examination of mRNA accumulation of defence genes in Aradopsis thaliana infested by O. ramosa, expression of several genes mediated by a JA-dependent pathway were activated by O. ramosa infestation whereas genes mediated by a SA-dependent pathway were not (Vieira Dos Santos et al., 2003a, b). Similarly, by using transgenic tobacco containing a promoter:GUS fusion, PR-1a, an indicator gene of the SA-dependent pathway induction, was not expressed by O. aegyptiaca infestation (Griffitts et al., 2004). Thus, it is likely that host plants induce a JA-dependent pathway rather than a SA-dependent pathway in response to Orobanche infestation. Activation of the JA-dependent pathway induced by Orobanche infestation are assumed to be insufficient for the inhibition of Orobanche parasitism because the exogenous application of JA analogues did not promote inhibition. Meanwhile, it may have been unnecessary for Orobanche to acquire the ability to overcome the induced resistance by SA during evolution because SA-mediated defence is an unusual response in the normal host–parasite interaction. It is assumed that the effectiveness of SA treatment on inhibition of the Orobanche parasitism is caused by the discordance between SA- and Orobanche-inducible responses.
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ACKNOWLEDGEMENTS |
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A part of this study was supported by Grants-in-Aid for Scientific Research (15830079, 1820810) from the Japanese Society for Promotion of Science (JSPS), and a grant for Eminent Research at Utsunomiya University.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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